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Article Sediment Carbon Variations in the Lagoon and Other Transitional Water Systems of the Northern Adriatic Sea

Adriano Sfriso 1,* , Alessandro Buosi 1 , Yari Tomio 1, Abdul-Salam Juhmani 1 , Stefania Chiesa 2,3, Marta Greco 2, Chiara Gazzola 2, Michele Mistri 4, Cristina Munari 4 and Andrea Augusto Sfriso 4

1 Department of Environmental Sciences, Informatics and Statistics (DAIS), University Ca’ Foscari Venice, Via Torino 155, 30170 (Ve), ; [email protected] (A.B.); [email protected] (Y.T.); [email protected] (A.-S.J.) 2 Department of Molecular Sciences and Nanosystems (DSMN), University Ca’ Foscari Venice, Via Torino 155, 30170 Mestre (Ve), Italy; [email protected] (S.C.); [email protected] (M.G.); [email protected] (C.G.) 3 Italian Institute for Environmental Protection and Research (ISPRA), Via Vitaliano Brancati 48, 00144 Rome, Italy 4 Department of Chemical and Pharmaceutical Sciences, University of Ferrara, Via Fossato di Mortara 17, 44121 Ferrara, Italy; [email protected] (M.M.); [email protected] (C.M.); [email protected] (A.A.S.) * Correspondence: [email protected]; Tel.: +39-041-234-8529

 Received: 10 November 2020; Accepted: 4 December 2020; Published: 6 December 2020 

Abstract: The concentrations of inorganic, organic and total carbon, and some sedimentary parameters (sediment density, fines, pH, and shell fragments), have been analyzed in surface sediments of the Venice Lagoon since 1987. Environmental scenarios, characterized by different anthropogenic impacts, have been considered, especially in the central basin where more information is available. Data collected in 2009 in the lagoons and ponds of Po Delta, in Comacchio Valleys and Pialassa della Baiona have been also considered and analyzed together with those recorded in the whole Venice Lagoon in 2011. The results show a strong correlation of the inorganic carbon (Cinorg) with the carbonatic or siliceous origins of the sediments and changes of both Cinorg and organic carbon (Corg) according to different anthropogenic impacts, especially eutrophication and clam-fishing activities. Higher sediment density, grain-size, and pH were associated to good-high ecological conditions and the higher presence of inorganic carbon of biological origin (shell fragments and calcified macroalgal fragments). Conversely, Corg, which is associated to eutrophic conditions, was strongly affected by the sediment disturbance and the presence of high concentrations of bivalves which enhance its consumption.

Keywords: carbon concentrations; surface sediments; anthropogenic impacts; environment resilience; transitional environments; Venice Lagoon; Po Delta; Comacchio Valleys; Pialassa della Baiona

1. Introduction Transitional Water Systems (TWS) are water bodies (lagoons, ponds, deltas, estuaries, fjords) with wide ecological features ranging from marine to freshwater conditions. They can be strongly affected by freshwater inputs (i.e., Po delta lagoons and ponds in Italy [1,2]), be almost completely devoid (i.e., Mar Menor in Spain [3]) or present intermediate conditions (i.e., Venice Lagoon, in Italy,[4]). TWS are under severe stress conditions from both natural and anthropogenic pressures that affect the ecological status and organism communities, including salinity [5]), nutrient/pollutant inputs [6,7], harboring [8],

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inputs [6,7], harboring [8], and fishing activities [9,10]. However, a high water renewal can strongly andmitigate fishing these activities impacts, [9,10 triggering]. However, a rapid a high enviro waternmental renewal recovery can strongly [7]. Changes mitigate of these nutrients impacts, and triggeringcarbon concentrations a rapid environmental in surface recovery sediments [7]. Changes are the of results nutrients of and both carbon human concentrations impacts and in surfacenatural sedimentsecosystem are resilience. the results When of both anthropogenic human impacts andpres naturalsures reduced, ecosystem the resilience. sedimentary When anthropogenicsystem would pressuresrecover, influencing reduced, the the sedimentary vegetation [11] system and would the benthic recover, [12,13] influencing and fish thefauna vegetation [14,15]. [11] and the benthicDespite [12,13] the and wide fish faunaliterature [14,15 concerning]. nutrient [6,7,10], different pollutant concentration [16– 18],Despite and biota the changes wide literature [12,13], the concerning information nutrient on ca [6rbon,7,10 concentrations], different pollutant is nowadays concentration very scarce [16– 18[17–], and19]. biota changes [12,13], the information on carbon concentrations is nowadays very scarce [17–19]. Therefore,Therefore, the the aims aims of of the the present present study study were were mainly mainly two: two: (i) (i) to to describe describe the the spatial spatial and and temporal temporal variationsvariations of of carbon carbon concentrations concentrations (total, (total, inorganic, inorga andnic, organic)and organic) in the in surface the surface sediment sediment of the Venice of the LagoonVenice sinceLagoon 1987 since and 1987 (ii) to and compare (ii) to compare the data fromthe data the Venicefrom the Lagoon Venice with Lagoon those with collected those incollected other TWSsin other in the TWSs northern in the Adriaticnorthern Sea Adriatic (Italy). Sea (Italy).

2.2. Materials Materials and and Methods Methods

2.1.2.1. Description Description of of Study Study Areas Areas and and Sampling Sampling Campaigns Campaigns TheThe Venice Venice Lagoon, Lagoon, located located in in the the north-western north-western Adriatic Adriatic Sea, Sea, is is the the most most studied studied TWS TWS of of the the 2 MediterraneanMediterranean Sea. Sea. It It covers covers an an area area of ca.of ca. 549 549 km kmaccounting2 accounting for ca.for 39%ca. 39% of the of total the total Italian Italian TWSs TWSs [11] 2 and[11] has and a waterhas a water surface surface of ca. of 432 ca. km 432(Figure km2 (Figure1). 1).

Figure 1. Main Transitional Water Systems (TWS) of the North-western Adriatic Sea. Figure 1. Main Transitional Water Systems (TWS) of the North-western Adriatic Sea. The mean depth of the Venice Lagoon is ca. 1.2 m on the mean tide level: it reaches 15–20 m in the canals,The 1–2.5 mean m in depth the water of the bodies Venice and Lagoon a few is centimeters ca. 1.2 m on in the shallowermean tide areas.level: it Water reaches circulation 15–20 m in in the canals, 1–2.5 m in the water bodies and a few centimeters in the shallower areas. Water circulation

Water 2020, 12, 3430 3 of 13 the Venice Lagoon is mainly driven by tidal action [19] which enables the renewal of about 60% of the total lagoon water every 12 h [20]. Residence time varies over the lagoon and with meteorological conditions, with average values ranging from few days, in the areas close to the inlets, to 40 days in the inner, chocked areas [21]. Morphological barriers (Malamocco- canal at South, and the salt marshes of and at North) divide the lagoon into three basins differing from the hydrological ones whose watersheds shift according to tides and winds. The Venice Lagoon is also characterized by strong 3 1 marine conditions resulted from the high water exchange (ca 19,000 m s− ) with the sea, in comparison 3 1 with negligible freshwater inputs of 34.5 m s− [22]. Since 2003, the research team at the Marine Ecology Lab, Ca‘ Foscari University of Venice (Italy) has collected data on the Carbon of the superficial sediments in the entire lagoon. Sampling campaigns were carried out in 2003 (165 stations), 2011 (118 stations), 2014 and 2018 (88 stations), and in the late spring–early summer period. In this paper, the concentrations recorded in 85 common stations have been analyzed and compared. In addition, for the central lagoon (132 km2), carbon mapping dates back to 1987 (35 stations) and was repeated in 1993, 1998, 2003, 2011, 2014, and 2018. This wide temporal scale allowed us to analyze the carbon concentrations in the various events that have characterized the lagoon over the last 40 years: the macroalgal dominance (1987) [4,23]; the macroalgal decline (1993) [24]; the intense Manila clam (Ruditapes philippinarum Adams Reeve) fishing activities (1998–2003) [10]; the clam-fishing decline (2011) [7]; and the reduction of anthropogenic impacts and the beginning of the lagoon environmental recovery (2014–2018) [7]. The Po Delta includes a wide water surface (ca. 204 km2) divided into many lagoons and ponds with depth ranging from 0.5 to 2.5 m, according to the water body. Salinity is very variable depending on the proximity and flow of the river mouths. Hard substrata are rare and mainly represented by some oyster beds scattered on the bottoms or stone embankments. Clam-farming and clam-fishing activities, unlike the Venice Lagoon where they declined sharply [7], are the main resources of the basins, resulting in high sediment resuspension with severe environmental consequences. The main primary producer of Po Delta is phytoplankton, whereas the free-floating nitrophilic macroalgae, especially Ulvaceae, Gracilariaceae, and Solieriaceae dominate the areas with lower anthropogenic impact. The beds of the aquatic angiosperm Ruppia cirrhosa (Petagna) Grande present until the 1990s has now completely disappeared [25]. The ecological conditions were ranging from poor to bad [25]. For these lagoons, there is little information and these are the only data available for the carbon species. Samples of surface sediments were collected in 2009 in 20 stations (3 at Caleri, 2 at Marinetta, 2 at Vallona, 3 at Barbamarco, 3 at Canarin, 4 at Scardovari, and 3 at Goro) during late spring–early summer period. The Comacchio Valleys are a complex of shallow coastal ponds of approximately 110 km2 which have slight exchange with the sea through two small channels. The freshwater input from the Reno River and the consequence of anthropogenic impacts like eel farming resulted in the shift of the ecological status from good ecological conditions dominated by aquatic angiosperms and macroalgae of high ecological value to a degraded and homogeneous basin dominated by phytoplankton and picocyanobacterial blooms of poor status ([26] and references therein). Contrary to the other TWS studied in this paper, water exchange with the sea is completely negligible and does not allow an improvement in the ecological status. Regarding surface sediments, no other carbon species information is available for this environment. Due to the homogeneity of the ecological conditions present throughout the basin, in 2009, samples of surface sediments were only collected in two stations during late spring–early summer period. The Pialassa della Baiona pond is a shallow basin (mean depth: 60 cm) of approximately 11 km2 connected with the Adriatic Sea through an artificial canal linked to the Ravenna harbor. Freshwater inputs, coming from a network of channels draining an intensively cultivated area, are negligible. The basin is colonized by abundant populations of macroalgae, especially the non-indigenous species Water 2020, 12, 3430 4 of 13

Agarophyton vermiculophyllum (Ohmi) Gurgel, J.N. Norris et Fredericq [27], and the ecological status is poor [28]. Moreover, this TWS has been little studied and no other information is available. Samples of surface sediments were collected in 2009 in three stations during late spring–early summer period.

2.2. Carbon Determination in Sediment The top 5 cm sediment layer was sampled by a Plexiglas corer (i.e., 10 cm). Three subsamples were collected in each station and mixed together. One subsample was retained for carbon analyses and another for the determination of the sediment grain-size and density. Both subsamples were stored at 20 C until the laboratory analyses. − ◦ Freeze-dried sediment samples were pulverized using a sediment mill (Fritsch Pulverisette, Idar-Oberstein, Germany). The concentration of total carbon (Ctot) was measured by a CHNS Analyzer (Vario-MICRO, Elementar CHNS, Thermo Fisher Scientific Inc., Milano, Italy) whereas inorganic carbon (Cinorg) was determined after samples combustion at 440 ◦C for 2 h [29] in order to eliminate most of the organic matter with negligible loss of carbonates [30]. Organic carbon (Corg) was determined by difference. All analyses were performed in duplicate in two different days in order to obtain an accuracy >95%. The quality and accuracy of quantitative analyses were assured by analyzing a certified reference material (Soil standard Ah, Carbon concentration: 7.44% 0.1) obtained from the ± National Institution of Standards and Technology NIST (USA). For sediments with high carbonate content (50–70%) as those present in the Venice Lagoon, heat combustion (440 ◦C) resulted to yield the closest measured concentrations of carbon, compared to those obtained with the acidification method described previously [31]. Both methods are affected by systematic errors arising from the elimination of Corg and Cinorg, but the combustion method is preferable, because the acidified samples may result in damaging of some parts of the CHNS-Analyzer. The concentrations of the carbon species 3 were reported in mg DWT cm− after normalization with the sediment amount per surface unity 1 (dry sediment density). Non-normalized data, expressed in mg g− dwt, are reported in Tables S1 and S2 in the Supplementary Material.

2.3. Sediment Characteristic Determination The determination of the pH (accuracy 0.015 units) of surface sediments (5 cm sediment top ± layer) was determined in field using a portable pH-meter (pH meter PH25 + CRISON). Dry sediment 3 density (g DWT cm− ) was determined in laboratory by sediment desiccation at 110 ◦C in tared crucibles of 20–30 mL. The percentage of fines (fraction < 63 µm) was obtained by wet sieving ca. 50 g of dried sediment throughout Endecotts sieves (ENCO Scientific Equipment, (Venice), Italy). All analyses were performed in duplicate. The amount of shell fragments was determined by sieving the dry sediment throughout a sieve of 1 mm before sediment grinding.

2.4. Statistical Analyses One-way analysis of variance (ANOVA) was applied to test differences of sediment parameter in different monitoring periods. Differences were considered significant when p < 0.05. Prior to the analyses, the distribution of each variable was checked for normality and homogeneity of variance by the Kolmogorov–Smirnov test (p < 0.05). Non-parametric Spearman’s coefficients (p < 0.05) highlighted the correlations among environmental parameters using STATISTICA 7.1 (StatSoft srl). The principal component analysis (PCA) analyzed the multivariate patterns of the matrix of 113 cases (stations) in response to the independent variables (shell fraction, sediment density, fines, inorganic, and organic carbon concentrations). Besides, the PCA transposed matrix was created to compare the relationship among the stations of the Venice Lagoon, the Po Delta, Comacchio Valleys, and Pialassa della Baiona. WaterWater2020 2020,,12 12,, 3430x FOR PEER REVIEW 55 of 1314

3. Results 3. Results 3.1. Carbon Determination and Sediment Characteristics 3.1. Carbon Determination and Sediment Characteristics The mean values of the carbon species (Ctot, Cinorg, Corg) concentrations and the superficial sedimentThe mean parameters values ofcollected the carbon in speciesthe studie (Ctot,d Cinorg,TWS are Corg) reported concentrations in Figure and 2 theand superficial Table S1 sediment(Supplementary parameters Material). collected Total in the carbon studied was TWS almost are reportedfive times in higher Figure 2(72.3 and mg Table cm S1−3 dwt) in Supplementary in the Venice 3 Material.Lagoon than Total carbonin the wasother almost TWSs five (14.5–16.2 times higher mg (72.3 cm− mg3 dwt), cm− mainlydwt) in thedue Venice to the Lagoon highest than Cinorg in the 3 3 otherconcentration TWSs (14.5–16.2 (59.4 mg mg cm cm−3− dwt).dwt), Similarly, mainly due in tothe the Venice highest Lagoon, Cinorg Corg concentration (12.9 mg ( 59.4cm−3mg dwt) cm was− dwt also). 3 Similarly,markedly inhigher the Venice than in Lagoon, the other Corg TWSs, (12.9 with mg cmconcen− dwt)trations was alsomore markedly than 2 times higher higher than than in the those other of 3 TWSs,the Po withDelta concentrations (5.8 mg cm−3 moredwt) and than 46–55% 2 times higher thanthan thosethe concentrations of the Po Delta in (5.8 Pialassa mg cm della− dwt) Baiona and 46–55%and Comacchio higher than Valleys, the concentrations respectively. in Pialassa della Baiona and Comacchio Valleys, respectively.

FigureFigure 2.2. AverageAverage values values of of the the carbon carbon species species (Ctot, (Ctot, Cinorg, Cinorg, Corg) Corg) and sedimentand sediment parameters parameters (pH, fines,(pH, dryfines, density, dry density, shell fragments) shell fragments) in the studiedin the studied TWSs. TWSs.

TheThe averageaverage pHpH valuesvalues ofof superficialsuperficial sedimentssediments ofof thethe VeniceVenice LagoonLagoon andand PialassaPialassa delladella BaionaBaiona werewere similarsimilar (7.41–7.40),(7.41–7.40), whereaswhereas thethe lowerlower meanmean value was recorded in the Comacchio Valleys (7.31) (Figure(Figure2 2).). This This was was strictly strictly related related to to the the lower lower percentage percentage of of fines fines (57%) (57%) and and sediment sediment dry dry density density −33 (0.59(0.59 gg dwtdwt cm cm− )) ofof thesethese TWSs.TWSs. Furthermore,Furthermore, the the lowest lowest shell shell fragments fragments percentage percentage was was observed observed in thein the Po DeltaPo Delta lagoons lagoons and ponds and ponds (1.90%), (1.90%), while the wh highestile the percentagehighest percentage was detected was in detected the Comacchio in the ValleysComacchio (22.3%) Valleys (Figure (22.3%)2). (Figure 2).

3.2.3.2. Carbon Variations inin thethe VeniceVenice LagoonLagoon (2003–2018)(2003–2018) TheThe concentrationsconcentrations ofof thethe carboncarbon speciesspecies (Ctot,(Ctot, Cinorg,Cinorg, Corg)Corg) inin surfacesurface sedimentssediments ofof thethe wholewhole VeniceVenice Lagoon Lagoon were were recorded recorded in in di differentfferent periods periods (2003; (2003; 2011; 2011; 2014 2014 and and 2018) 2018) (Figure (Figure3 and 3 and Table Table S2 inS2 Supplementaryin Supplementary Material). Material).

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FigureFigure 3.3.( a()a) Average Average values values of theof carbonthe carbon concentrations concentratio recordedns recorded in the surfacein the sedimentssurface sediments (85 stations) (85 ofstations) the whole of the Venice whole Lagoon. Venice Data Lagoon. were Data normalized were no takingrmalized into taking account into the account amount the of amount dry sediment of dry 3 −3 (drysediment density) (dry for density) volume for unit volume (b) and unit expressed (b) and expressed in mg dwt in cm mg− . dwt cm .

TheThe averageaverage CorgCorg concentrationsconcentrations (Figure(Figure3 3a)a) showed showed an an increasing increasing trend trend from from 2003 2003 (6.2 (6.2 mg mg dwt dwt 3 3 cmcm−−3)) during during the the intense intense clam-fishing clam-fishing activities activities to to2018 2018 (15.6 (15.6 mg mg dwt dwt cm− cm3) when− ) when these these activities activities were werenegligible. negligible. TheThe meanmean CorgCorg didifferencefference contributedcontributed significantlysignificantly toto increaseincrease thethe averageaverage concentrationconcentration ofof CtotCtot 3 3 thatthat changedchanged fromfrom 6565 mgmg dwt dwt cm cm−−3 (2003)(2003) toto 71.771.7 mgmgdwt dwt cm cm−−3 (2018).(2018). Indeed, thethe concentrationsconcentrations ofof CinorgCinorg werewere quitequite similar,similar, rangingrangingfrom from56.1 56.1to to 59.559.5 mgmg cmcm33.. In parallel, sediment density (Figure3 3b)b) 3 increasedincreased fromfrom 0.930.93 toto 1.051.05 mgmg cmcm−−3 with loss of the fine fine fraction. TheThe didifferencefference ofof CorgCorg amongamong thethe consideredconsidered yearsyears waswas highlyhighly significantsignificant (one-way ANOVA) betweenbetween 2003 and the other years: 2011, 2011, 2014, 2014, and and 2018 2018 (p (p << 0.001,0.001, Table Table 1).1). A A significant significant difference di fference (p (

TableTable 1.1.One-way One-way ANOVA ANOVA analysis analysis between between the dithefferent different sampling sampling periods; periods; n.s.: not n.s.: significant not significant values. values. One-Way ANOVA CtotOne-Way ANOVA Cinorg Corg

Ctot Cinorg Corg15 2003–2011 p < 0.050 n.s. p < 3.26 10− × −15 2003–20112003–2014 p

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Figure 4. Distribution maps of Ctot and Corg in the surface sediments of the whole Venice Lagoon.

The measurements of carbon in the central part of the Venice Lagoon referred to recent years (2003–2018) were then merged with three additional previous campaigns, carried out in 1987, 1993, and 1998 (Figure 5 and Table S3 in Supplementary Material). Figure 4. Distribution maps of Ctot and Corg in the surface sediments ofof thethe wholewhole VeniceVenice Lagoon.Lagoon.

The measurements of carbon in the central part of the Venice Lagoon referred to recent years (2003–2018) were then merged with three additional previous campaigns, carried out in 1987, 1993, and 1998 (Figure 5 and Table S3 in Supplementary Material).

Figure 5.5. (a(a)) Average Average values values of theof the carbon carbon concentrations concentratio recordedns recorded in the surfacein the surface sediments sediments (35 stations) (35 ofstations) the central of the Venice central Lagoon Venice during Lagoon diff duringerent periods. different (b )periods. Amount (b of) Amount dry sediment of dry (dry sediment density) (dry for volumedensity) unit.for volume unit.

3 In 1987,1987, Ctot Ctot and and Corg Corg concentrations concentrations were were 74.0 74.0 and 8.9and mg 8.9 dwt mg cm dwt− , respectively.cm−3, respectively. Organic Organic carbon Figure 5. (a) Average3 values of the carbon concentrations recorded in the surface sediments (35 3 dropped to 5.9 mg cm− in 1998,−3 whereas, in the following years, it increased to up to 13.9 mg cm− carbonstations) dropped of the to 5.9central mg cmVenice in La1998,goon whereas, during different in the following periods. ( byears,) Amount it increased of dry sediment to up to (dry 13.9 mg incm 2018−3 in 2018 (Figure (Figure5a). Since 5a). Since 2011, 2011, Corg Corg increased increased significantly, significantly, whereas whereas Ctot rangedCtot ranged between between 86.0 and86.0 density) for volume3 unit. 87.5and 87.5 mg dwtmg cmdwt− cm. The−3. The dry dry density density of surface of surface sediments sediments (Figure (Figure5b) followed 5b) followed the same the same trend trend of Ctot of increasing from 1987 to 2018, due to the loss of the fine fraction. Ctot increasingIn 1987, Ctot from and 1987 Corg to 2018, concentrations due to the losswere of 74.0 the fineand fraction.8.9 mg dwt cm−3, respectively. Organic The analysis of variance (one-way ANOVA) revealed that Corg concentrations were significantly carbonThe dropped analysis to 5.9of mgvariance cm−3 in (one-way1998, whereas, ANOVA) in the followingrevealed years,that Corgit increased concentrations to up to 13.9 were mg different (p < 0.05; p < 0.001) during the majority of the sampling periods (Table2), whereas no significantlycm−3 in 2018 (Figuredifferent 5a). (p Since< 0.05; 2011, p < Corg0.001) increased during the significantly, majority of whereas the sampling Ctot ranged periods between (Table 86.0 2), significant differences were recorded for Ctot and Cinorg, except the significant difference between whereasand 87.5 mgno dwtsignificant cm−3. The differences dry density were of surfacerecorded sediments for Ctot (Figure and Cinorg, 5b) followed except the the same significant trend of 1987 and 2011 for the Cinorg concentration. differenceCtot increasing between from 1987 1987 and to 20112018, for due the to Cinorgthe loss concentration. of the fine fraction. 3.3. CarbonThe analysis Variations of in allvariance TWSs (one-way ANOVA) revealed that Corg concentrations were significantly different (p < 0.05; p < 0.001) during the majority of the sampling periods (Table 2), whereasThe statisticalno significant analysis differences (non-parametric were recorded Spearman’s for coeCtotffi cients)and Cinorg, between except the stations the significant of all the considereddifference between TWSs showed 1987 and a high2011 numberfor the Cinorg of positive concentration. and inverse correlations between the carbon species and the considered parameters and between the same environmental parameters (Table3). Among them, the negative correlations between fines and dry density (r 0.65) and fines and pH ≤ − (r 0.59) and the positive correlations between dry density and pH (r 0.53) and dry density and ≤ − ≤ Cinorg (r 0.53) are particularly relevant. ≤

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Table 2. Statistical correlations (p-value) between carbon species (Ctot, Corg and Cinorg) during different sampling periods in the central part of the Venice Lagoon; n.s.: not significant.

One-Way ANOVA Ctot Cinorg Corg 1987–1993 n.s. n.s. 0.042 1987–1998 n.s. n.s. 2.49 10 4 × − 1987–2003 n.s. n.s. 0.026 1987–2011 n.s. 0.041 n.s. 1987–2014 n.s. n.s. 3.13 10 4 × − 1987–2018 n.s. n.s. 3.69 10 6 × − 1993–1998 n.s. n.s. n.s. 1993–2003 n.s. n.s. n.s. 1993–2011 n.s. n.s. 8.59 10 4 × − 1993–2014 n.s. n.s. 1.98 10 7 × − 1993–2018 n.s. n.s. 6.14 10 9 × − 1998–2003 n.s. n.s. n.s. 1998–2011 n.s. n.s. 2.10 10 6 × − 1998–2014 n.s. n.s. 7.84 10 11 × − 1998–2018 n.s. n.s. 1.14 10 11 × − 2003–2011 n.s. n.s. 5.42 10 4 × − 2003–2014 n.s. n.s. 4.08 10 7 × − 2003–2018 n.s. n.s. 4.70 10 9 × − 2011–2014 n.s. n.s. n.s. 2011–2018 n.s. n.s. 8.03 10 4 × − 2014–2018 n.s. n.s. n.s

Table 3. Non-parametric Spearman’s coefficients between carbon compounds and some parameters of surface sediments of all the considered lagoons and ponds. In red, significant values: p < 0.05 for r 0.19. ≥ Spearman’s Non-Parametric Coefficients p < 0.05 per r 0.19 ≥ pH Fines Shells Dry Density Corg Cinorg Ctot pH 1.00 Fines 0.59 0.59 − − Shells 0.27 0.34 1.00 − Dry density 0.53 0.65 0.07 1.00 − Corg 0.25 0.32 0.26 0.42 1.00 − − Cinorg 0.19 0.04 0.26 0.45 0.05 1.00 − Ctot 0.01 0.08 0.31 0.20 0.35 0.85 1.00

The principal component analysis (PCA) of the first two components applied to the whole stations sampled in 2009 in the Po Delta, Comacchio Valleys, and Pialassa della Baiona, and in 2011, the closest date of those sampled in Venice Lagoon, are shown in Figure6a. The first two components explained the 61.1% of the total variance and the four sediment parameters, namely: pH, dry density, fines, and shell fragments showed a loading >0.7. The explained variance increased to 79.6% by considering three components. In addition, PCA highlighted the affinity among parameters confirming the results of the correlations coefficients: pH and the sediment density were associated to the concentration of Cinorg and the presence of shell fragments, whereas Corg was clustered in the same side of fines. Water 2020, 12, x FOR PEER REVIEW 9 of 14

explained the 61.1% of the total variance and the four sediment parameters, namely: pH, dry density, fines, and shell fragments showed a loading >0.7. The explained variance increased to 79.6% by considering three components. In addition, PCA highlighted the affinity among parameters confirming the results of the correlations coefficients: pH and the sediment density were associated to the concentration of Cinorg and the presence of shell fragments, whereas Corg was clustered in Water 2020, 12, 3430 9 of 13 the same side of fines.

Figure 6. a Figure 6. ((a)) Principal Principal component component analysis analysis (PCA) (PCA) amon amongg carbon species and surface sediment characteristics. Red small circles represent values of loading >0.7. Large circles show the different characteristics. Red small circles represent values of loading >0.7. Large circles show the different parameters clustering associated to bad (red) or good (blue) ecological conditions. (b) PCA of the parameters clustering associated to bad (red) or good (blue) ecological conditions. (b) PCA of the transposed matrix to highlight the station associations. The different colors show different TWSs. In blue: transposed matrix to highlight the station associations. The different colors show different TWSs. In Venice Lagoon; in black: lagoons and ponds of the Po Delta; in green: Pialassa della Baiona; in red: blue: Venice Lagoon; in black: lagoons and ponds of the Po Delta; in green: Pialassa della Baiona; in Comacchio Valleys. red: Comacchio Valleys. The PCA of the transposed matrix applied to the same parameters and stations (Figure6b) shows The PCA of the transposed matrix applied to the same parameters and stations (Figure 6b) shows the clustering among the stations of the different TWSs. All the stations of the Venice Lagoon and the clustering among the stations of the different TWSs. All the stations of the Venice Lagoon and Po Po Delta are evenly distributed in the biplot showing a high heterogeneity and partially overlap, Delta are evenly distributed in the biplot showing a high heterogeneity and partially overlap, whereas the stations of the Comacchio Valleys and Pialassa della Baiona are clustered in the lower side whereas the stations of the Comacchio Valleys and Pialassa della Baiona are clustered in the lower of the biplot showing minor differences. side of the biplot showing minor differences. 4. Discussion 4. Discussion Carbon concentrations in surface sediments showed a close relationship with sediment origin and theCarbon anthropogenic concentrations activities in surface that a ffsedimentsected the TWSsshowed of a the close Northern relationship Adriatic with Sea. sediment Indeed, origin in the northernand the anthropogenic basin of the Venice activities Lagoon, that during affected the the periods TWSs of of the the 16th Northern and 17th Adriatic centuries, Sea. the Indeed, main in rivers the th th werenorthern diverted basin into of the the Venice sea in Lagoon, order to avoidduring the the landfill periods of of the the lagoon 16 and [32 17], and centuries, some of the them main enriched rivers thewere sediments diverted withinto the high sea amounts in order ofto carbonatesavoid the land [17].fill Inorganic of the lagoon carbon [32], was and transported some of them and enriched released intothe sediments the lagoon with by rivers high Piaveamounts and of Brenta carbonates originating [17]. fromInorganic the Dolomites carbon was (i.e., transported the limestone and mountain released systeminto the located lagoon in by the rivers north-eastern Piave and Alps). Brenta The orig TWSsinating located from southern the Dolomites of the Venice (i.e., Lagoon the limestone instead weremountain formed system by the located Adige in and the Ponorth-eastern rivers originating Alps). inThe the TWSs central-western located southern Alps andof the consist Venice mainly Lagoon of siliceousinstead were minerals. formed These by the diff Adigeerent contributionsand Po rivers oforiginating carbonates in explain the central-western the decreasing Alps concentrations and consist ofmainly Cinorg of andsiliceous Ctot observedminerals. fromThese North different to South contributions in the TWS of incarbonates the western explain coasts the of decreasing the North Adriaticconcentrations Sea, as of previously Cinorg and reported Ctot observed in a study from [33] North that described to South richer in the silicate-related TWS in the western elements coasts in the of sedimentsthe North Adriatic from the Sea, southern as previously lagoon in reported comparison in a withstudy the [33] calcite that /describeddolomite richricher sediments silicate-related of the northernelements lagoon.in the sediments from the southern lagoon in comparison with the calcite/dolomite rich sedimentsApart of from the this,northern the concentrationslagoon. of the Corg seem to be affected mainly by the presence of macrophytes,Apart from the this, abundance the concentrations of clams, and of by the clam-fishing Corg seem activities. to be affected Notably, mainly the presence by the presence of massive of angiospermmacrophytes, meadows the abundance and macroalgal of clams, beds and in by Venice clam-fishing Lagoon enrichedactivities. the Notably, sediments the withpresence organic of mattermassive [34 angiosperm,35]. To these meadows should beand added macroalgal the considerable beds in Venice carbon Lagoon sequestration enriched rates the sediments of salt-marshes with and reeds from freshwater flooded areas (psu < 9) mainly colonized by Phragmites australis (Cav.) Trin. ex Steud. whose root-rhizome and stem fragments are still clearly recognizable in the peat deposits of the sediments alongside the landward area of the southern Venice Lagoon [36,37] and in the surrounding watershed lands [38]. These areas evolved over the last five centuries from palustrine reed/salt-marsh dominated environments toward depositional tidal-flat/subtidal environments storing Water 2020, 12, 3430 10 of 13 elevated Corg concentrations in the sediments [36,37]. Despite the intense clam fishing activities in these areas, the high degree of confinement allowed the retention of the fine fraction resuspended preserving a higher carbon content in the superficial sediments. A similar reasoning can be developed for the Corg-rich areas of the Northern Lagoon near the mouth of the River Dese where reeds and salt-marshes are constantly evolving. Instead, the other TWS are characterized by the absence of aquatic angiosperms that favor the sediment enrichment with organic matter. However, due to the lower dry density recorded in the 3 lagoons of the Po Delta (0.86 g dwt cm− ), Pialassa della Baiona, and Comacchio Valleys (0.59 g 3 dwt cm− ), the mean Corg concentrations in surface sediments resulted further reduced (Figure2). However, Comacchio Valleys were completely deprived of vegetation, whereas the lagoons and ponds of the Po Delta, in spite of the high organic inputs from the Po river, were affected by anthropogenic activities. Indeed, in the latter TWSs, the availability of Corg was reduced both by (i) high concentration 2 of clams (on average 3–6 kg m− [7]) that filtered the organic matter present in the water column near the surface sediment, and (ii) sediment disturbance caused by clam-fishing with hydraulic and mechanical dredges, which mixed the first 10–15 cm of surface sediment releasing nutrients and organic matter in the water column [10]. The above-mentioned impacts are clearly observed by examining the data of carbon distribution obtained in the central basin of the Venice Lagoon, during different times: (a) 1987: The lagoon was dominated by a massive algal growth with a biomass ranging from 5 to 20 kg 2 2 2 fwt m− in 65 km out of 132 km of the whole basin [35]); (b) 1993: Macroalgal biomass decreased 2 from 4.78 to 0.69 kg m− fwt [7,24,35]; (c) 1998: Clam-fishing occurred in the entire central lagoon and 2 the macroalgal biomass decreased further to 0.11 kg fwt m− with significant decrease of nutrient concentrations in surface sediments [10]; (d) 2003: Clam-fishing reached its excessive impact and lasted 1 until 1999–2000 when clam production reached 40,000/60,000 tons y− [39]; (e) 2011: Clam-fishing 1 declined to ca. 2000 tons y− and the lagoon showed a progressive ecological recovery [7]; (f) 2014: Aquatic angiosperms and macroalgae of high ecological value started to recolonize the lagoon [7]; and (g) 2018: The lagoon recovery continually increased and the aquatic angiosperm Ruppia cirrhosa, which disappeared in the open lagoon during the massive macroalgal development [40], started to re-colonize the choked areas. In 1997, surface sediments of the central part of the Venice Lagoon showed the lowest dry 3 3 density (0.99 g cm− ) and Corg was relatively high (8.9 mg cm− ) (Figure5). In the following years, 3 dry density progressively increased until 1.17 g cm− , due to the loss of the fine fraction [41,42]. 3 In 1998, Corg reached the minimum value (5.9 mg cm− ) when sediments were affected by intense 3 clam-fishing activities [10,12,41] (Figure5a). In 2003, Corg began to increase (7.0 mg cm − , Figure5a). In 2011, clam-fishing activities dropped significantly due to stock reduction and carbon concentrations consequently increased. In the subsequent years, Corg concentrations continuously increased due to lack of clams, the absence of sediment disturbance by clam-fishing activities, and the recolonization of macrophytes (mostly aquatic angiosperms and sensitive macroalgae) [7]. Eventually, either a high clam density or clam harvesting with sediment resuspension and fine fraction loss contributed significantly to Corg reduction as it was also recorded for the Po Delta lagoons, where the mean 3 Corg concentration was 7.0 mg cm− dwt (Figure2) and where intense clam fishing activities are regularly carried out. Sediment resuspension promotes biodegradation of sedimentary organic matter [43]; moreover, the disruption of organic carbon distribution due to clam mechanical fishing activities was previously reported by [44] on a study of the immediate effects of mechanical clam harvesting. Indeed, the concentrations of Corg were strongly correlated to sediment fines percentage, whereas Cinorg was associated to sediment density and pH (Table3). The positive correlation between Cinorg and pH (Table3) may be explained by the reduction or disappearance of crustose coralline algae at low pH values (6.7 8.0), and as a consequence, the loss of the sediment carbonate fraction, ≤ as previously described [45–47] for studies on volcanic marine CO2 vents in the sea around Ischia Island. Likewise, researchers [48] found that pH had a strong correlation with Cinorg produced from the small microcalcareus macroalgae belonging to the epiphytic genera Pneophyllum, Hydrolithon, and Melobesia, Water 2020, 12, 3430 11 of 13 which grow on the largest macroalgae and aquatic angiosperms of the Italian TWS. These taxa, under an acidic water column (pH < 7.93), were not able to grow, thus reducing significantly the production of carbonates trapped by these small algae and accumulated in surface sediments [48]. In extreme cases of acidic sediment (pH < 7.0), as in the canals of the historical center of Venice, the shells of bivalves and gastropods are not present, as they dissolve rapidly. On the other hand, Corg showed a high affinity for Fine sediments, nutrients, [10] and pollutants [49–51], due to the larger surface area of smaller sediment particles. Therefore, in the case of the Po Delta lagoons the high filtration due to the abundance of clam populations and intense clam-fishing activities, resulted in the re-suspension of high amounts of sediments and the decrease of the organic matter rich fine fractions. This scenario significantly lowered the Corg concentrations, as recorded in the Venice Lagoon between the 1990s and 2010 [10,41,42].

Supplementary Materials: The following are available online at http://www.mdpi.com/2073-4441/12/12/3430/s1, Table S1: Carbon concentrations in the lagoons and ponds of the North Western Adriatic Sea; Table S2: Sediment density and carbon concentrations in the Venice Lagoon during different scenarios: 2002, 2011, 2014, 2018; Table S3, Mean sediment density and carbon concentrations in the central Venice Lagoon during different scenarios. Author Contributions: Conceptualization, A.S., S.C., and M.M.; Formal analysis, A.B., Y.T., A.-S.J., M.G., C.G., and A.A.S; Funding acquisition, A.S.; Investigation, A.S.; Methodology, A.S. and S.C.; Supervision, A.S.; S.C., M.M., C.M., and A.A.S.; Visualization, A.S. and M.M.; Writing—original draft, A.S. and A.A.S.; Writing—review & editing, A.S., A.A.S., and S.C. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by Department funds. Acknowledgments: The authors thank ARPA of and Emilia Romagna Regions, which financed the data collection of some measurement campaigns and the anonymous referees who contributed to the improvement of the paper. Conflicts of Interest: The authors declare no conflict of interest.

References

1. Castaldelli, G.; Mantovani, S.; Welsh, D.T.; Rossi, R.; Mistri, M.; Fano, E.A. Impact of commercial clam harvesting on water column and sediment physicochemical characteristics and macrobenthic community structure in a lagoon (Sacca di Goro) of the Po River Delta. Chem. Ecol. 2003, 19, 161–171. [CrossRef] 2. Mistri, M.; Munari, C.; Pagnoni, A.; Chenet, T.; Pasti, L.; Cavazzini, A. Accumulation of trace metals in crayfish tissues: Is Procambarus clarkii a vector of pollutants in Po Delta inland waters? Eur. Zool. J. 2020, 87, 46–57. [CrossRef] 3. Velasco, J.; Lloret, J.; Millan, A.; Marin, A.; Barahona, J.; Abellan, P.; Sanchez-Fernandez, D. Nutrient and particulate inputs into the Mar Menor lagoon (SE Spain) from an intensive agricultural watershed. Water Air Soil Pollut. 2006, 176, 37–56. [CrossRef] 4. Sfriso, A.; Pavoni, B.; Marcomini, A.; Orio, A.A. Macroalgae, nutrient cycles and pollutants in the lagoon of Venice. Estuar. Coast. 1992, 15, 517–528. [CrossRef] 5. Kefford, B.; Dunlop, J.; Nugegoda1, D.; Choy, S. Understanding salinity thresholds in freshwater biodiversity, freshwater to saline transition. In Salt, Nutrient, Sediment and Interactions: Findings from the National River Contaminants Program; Land & Water Australia: Canberra, Australia, 2007; Chapter 2; pp. 9–28. 6. Solidoro, C.; Bandelj, V.; Bernardi, F.A.; Camatti, E.; Ciavatta, S.; Cossarini, G.; Facca, C.; Franzoi, P.; Libralato, S.; Melaku Canu, D.; et al. Response of the Venice Lagoon Ecosystem to Natural and Anthropogenic Pressures over the last 50 years. In Coastal Lagoons—Critical Habitats of Environmental Change; Kennish, M.J., Paerl, H.W., Eds.; CRC Press: Boca Raton, FL, USA, 2010; Chapter 19; pp. 483–511. 7. Sfriso, A.; Buosi, A.; Mistri, M.; Munari, C.; Franzoi, P.; Sfriso, A.A. Long-term changes of the trophic status in transitional ecosystems of the northern Adriatic Sea, key parameters and future expectations: The lagoon of Venice as a study case. Nat. Conserv. 2019, 34, 193–215. [CrossRef] 8. Trozzi, C.; Vaccaro, R. Environmental impact of port activities. In Maritime Engineering and Ports II; Brebbia, C.A., Olivella, J., Eds.; WIT Press: Rome, Italy, 2000; pp. 151–161. 9. Bartoli, M.; Nizzoli, D.; Viaroli, P.; Turolla, E.; Castaldelli, G.; Fano, E.A.; Rossi, R. Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 2001, 455, 203–212. [CrossRef] Water 2020, 12, 3430 12 of 13

10. Sfriso, A.; Facca, C.; Ceoldo, S.; Silvestri, S.; Ghetti, P.F. Role of macroalgal biomass and clam fishing on spatial and temporal changes in N and P sedimentary pools in the central part of the Venice lagoon. Oceanol. Acta 2003, 26, 3–13. [CrossRef] 11. Sfriso, A.; Buosi, A.; Facca, C.; Sfriso, A.A. Role of environmental factors in affecting macrophyte dominance in transitional environments: The Italian Lagoons as a study case. Mar. Ecol. 2017, 38, e12414. [CrossRef] 12. Pranovi, F.; Da Ponte, F.; Torricelli, P. Historical changes in the structure and functioning of the benthic community in the lagoon of Venice. Estuar. Coast. Mar. Sci. 2008, 76, 753–764. [CrossRef] 13. Pitacco, V.; Mistri, M.; Aleffi, I.F.; Lardicci, C.; Prato, S.; Tagliapietra, D.; Munari, C. Spatial patterns of macrobenthic alpha and beta diversity at different scales in Italian transitional waters (central Mediterranean). Estuar. Coast. Mar. Sci. 2019, 222, 126–138. [CrossRef] 14. Scapin, L.; Zucchetta, M.; Sfriso, A.; Franzoi, P. Predicting the response of nekton assemblages to seagrass transplantations in the Venice lagoon: An approach to assess ecological restoration. Aquat. Conserv. Mar. Freshw. Ecosyst. 2019, 29, 849–864. [CrossRef] 15. Cavraro, F.; Bettoso, N.; Zucchetta, M.; D’Aietti, A.; Faresi, L.; Franzoi, P. Body condition in fish as a tool to detect the effects of anthropogenic pressures in transitional waters. Aquat. Ecol. 2019, 53, 21–35. [CrossRef] 16. Giordani-Soika, A.; Perin, G. L’inquinamento della laguna di Venezia: Studio delle modificazioni chimiche e del popolamento sottobasale dei sedimenti lagunari negli ultimi vent’anni. Boll. Mus. Civ. St. Nat. Venezia 1974, 26, 25–68. 17. Cossu, A.; De Fraja-Frangipane, E. Stato delle Conoscenze Sullo Inquinamento Della Laguna di Venezia. In Progetto Venezia, Ministero dei Lavori Pubblici, Magistrato alle Acque; Consorzio Venezia Nuova: Venezia, Italy, 1985; Volume 4. 18. Consorzio Venezia Nuova; Magistrato alle Acque. Nuovi Interventi per la Salvaguardia di Venezia. Rapporto sullo Stato Attuale dell’Ecosistema Lagunare; Studio 1.3.9: Rapporto Finale; Consorzio Venezia Nuova Venezia: Venezia, Italy, 1990; p. 361. 19. Gaˇci´c,M.; Mosquera, I.M.; Kovaˇcevi´c,V.; Mazzoldi, A.; Cardin, V.; Arena, F.; Gelsi, G. Temporal variations of water flow between the and the open sea. J. Mar. Syst. 2004, 51, 33–47. [CrossRef] 20. Masiol, M.; Facca, C.; Visin, F.; Sfriso, A.; Pavoni, B. Interannual heavy element and nutrient concentration trends in the top sediments of Venice Lagoon (Italy). Mar. Poll. Bull. 2014, 89, 49–58. [CrossRef] 21. Cucco, A.; Umgiesser, G. Modeling the Venice Lagoon residence time. Ecol. Model. 2006, 193, 34–51. [CrossRef] 22. Zuliani, A.; Zaggia, L.; Collavini, F.; Zonta, R. Freshwater discharge from the drainage basin to the Venice Lagoon (Italy). Environ. Int. 2005, 31, 929–938. [CrossRef] 23. Sfriso, A.; Pavoni, B.; Marcomini, A.; Orio, A.A. Annual variation of nutrients in the lagoon of Venice. Mar. Poll. Bull. 1988, 19, 54–60. [CrossRef] 24. Sfriso, A.; Marcomini, A. Decline of Ulva growth in the lagoon of Venice. Bioresour. Technol. 1996, 58, 299–307. [CrossRef] 25. Sfriso, A.; Facca, C.; Bon, D.; Buosi, A. Macrophytes and ecological status assessment in the Po delta transitional systems, Adriatic Sea (Italy). Application of Macrophyte Quality Index (MaQI). Acta Adriat. 2016, 57, 209–226. 26. Munari, C.; Mistri, M. Ecological status assessment and response of benthic communities to environmental variability: The Valli di Comacchio (Italy) as a study case. Mar. Environ. Res. 2012, 81, 53–61. [CrossRef] [PubMed] 27. Sfriso, A.; Buosi, A.; Wolf, M.A.; Sfriso, A.A. Invasion of alien macroalgae in the Venice Lagoon, a pest or a resource? Aquat. Invasions 2020, 15, 245–270. [CrossRef] 28. Covelli, S.; Emili, A.; Acquavita, A.; Koron, N.; Fraganeli, J. Benthic biogeo-chemical cycling of mercury in two contaminated northern Adriatic coastal lagoons. Cont. Shelf Res. 2011, 31, 1777–1789. [CrossRef] 29. Schumacher, B.A. Method for the Determination of Total Organic Carbon (TOC) in Soil and Sediment; Ecological Risk Assessment Support Center, Office of Research and Development, US Environmental Protection Agency: Las Vegas, Nevada, 2002; pp. 1–2. 30. Kristensen, E.; Andersen, F.Ø. Determination of organic carbon in marine sediments: A comparison of two CHN analyzer methods. J. Exp. Mar. Biol. Ecol. 1987, 109, 15–23. [CrossRef] 31. Froelich, P.N. Analysis of organic carbon in marine sediments. Limnol. Oceanogr. 1980, 25, 564–572. 32. Miozzi, E. Venezia nei Secoli—La Laguna, Grafiche Trevisan, Castelfranco Veneto; Grafiche Trevisan, Castelfranco Veneto: Venice, Italy, 1968; Volume III, p. 543. Water 2020, 12, 3430 13 of 13

33. Frignani, M.; National, I.; Dinelli, E. Composition of Venice Lagoon sediments: Distribution, sources, settings and recent evolution. GeoActa 2001, 1, 1–14. 34. Sfriso, A.; Marcomini, A.; Pavoni, B. Relationship between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice lagoon. Mar. Environ. Res. 1987, 22, 297–312. [CrossRef] 35. Sfriso, A.; Facca, C. Distribution and production of macrophytes in the lagoon of Venice. Comparison of actual and past abundance. Hydrobiologia 2007, 577, 71–85. [CrossRef] 36. Roner, M.; D’Alpaos, A.; Ghinassi, M.; Marani, M.; Silvestri, S.; Franceschini, E.; Realdon, N. Spatial variation of salt-marsh organic and inorganic deposition and organic carbon accumulation: Inferences from the Venice lagoon, Italy. Adv. Water Resour. 2016, 93, 276–287. [CrossRef] 37. Roner, M.; Ghinassi, M.; Fedi, M.; Liccioli, L.; Bellucci, L.G.; Brivio, L.; D’Alpaos, A. Latest Holocene depositional history of the southern Venice Lagoon, Italy. Holocene 2017, 27, 1–14. [CrossRef] 38. Gambolati, G.; Putti, M.; Teatini, P.; Camporese, M.; Ferraris, S.; Gasparetto-Stori, G.; Nicoletti, V.; Silvestri, S.; Rizzetto, F.; Tosi, L. Peat Land Oxidation Enhances Subsidence in the Venice Watershed. Eos 2005, 86, 217–224. [CrossRef] 39. Boscolo Brusà, R.; Cacciatore, F.; Ponis, E.; Molin, E.; Delaney, E. Clam culture in the Venice lagoon: Stock assessment of Manila clam (Venerupis philippinarum) populations at a nursery site and management proposals to increase clam farming sustainability. Aquat. Living Resour. 2013, 26, 1–10. [CrossRef] 40. Sfriso, A. Ruppia maritima L. e Ruppia cirrhosa (Petagna) Grande (Helobiae, Spermatophyta) in laguna di Venezia. Lavori Soc. Ven. Sc. Nat. 2008, 33, 41–46. 41. Sfriso, A.; Facca, C.; Marcomini, A. Sedimentation rates and erosion processes in the lagoon of Venice. Environ. Int. 2005, 31, 983–992. [PubMed] 42. Sfriso, A.; Facca, C.; Ceoldo, S.; Pessa, G. Sedimentation rates, erosive processes, grain-size and sediment density changes in the lagoon of Venice. In Scientific Research and Safeguarding of Venice. Corila Research Program 2003 Results; Campostrini, P., Ed.; Multigraf: Spinea, Italy, 2005; Volume 3, pp. 203–213. 43. Aller, R.C. Mobile deltaic and continental shelf muds as suboxic, fluidized bed reactors. Mar. Chem. 1998, 61, 143–155. [CrossRef] 44. Pranovi, F.; Da Ponte, F.; Raicevich, S.; Giovanardi, O. A multidisciplinary study of the immediate effects of mechanical clam harvesting in the Venice Lagoon. ICES J. Mar. Sci. 2004, 61, 43–52. [CrossRef] 45. Porzio, L.; Garrard, S.L.; Buia, M.C. The effect of ocean acidification on early algal colonization stages at

natural CO2 vents. Mar. Biol. 2013, 160, 2247–2259. [CrossRef] 46. Kumar, A.; Abdelgawad, H.; Castellano, I.; Lorenti, M.; Delledonne, M.; Beemster, G.T.S.; Asard, H.; Buia, M.C.; Palumbo, A. Physiological and Biochemical Analyses Shed Light on the Response of Sargassum vulgare to Ocean Acidification at Different Time Scales. Front. Plant Sci. 2017, 8, 11–14. [CrossRef] 47. Foo, S.A.; Byrne, M.; Ricevuto, E.; Gambi, M.C. The carbon dioxide vents of Ischia, Italy, a natural System to assess impacts of ocean acidification on marine ecosystems: An overview of research and comparisons with other vent systems. Oceanogr. Mar. Biol. Annu. Rev. 2018, 56, 237–310. 48. Sfriso, A.; Buosi, A.; Wolf, M.A.; Sciuto, K.; Molinaroli, E.; Mistri, M.; Munari, C.; Moro, I.; Sfriso, A.A.

Microcalcareus seaweeds a sentinel of trophic changes and CO2 trapping in transitional waters. Ecol. Indic. 2020, 118, 1–10. [CrossRef] 49. Pavoni, B.; Calvo, C.; Sfriso, A.; Orio, A.A. Time trend of PCB concentrations in surface sediment from a hypertrophic, macroalgae populated area of the lagoon of Venice. Sci. Total Environ. 1990, 91, 13–21. [CrossRef] 50. Secco, T.; Pellizzato, F.; Sfriso, A.; Pavoni, B. The changing state of contamination in the lagoon of Venice. Part 1. Organic pollutants. Chemosphere 2005, 58, 279–290. [CrossRef][PubMed] 51. Bernardello, M.; Secco, T.; Pellizzato, F.; Chinellato, M.; Sfriso, A.; Pavoni, B. The changing state of contamination in the lagoon of Venice. Part 2: Heavy metals. Chemosphere 2006, 64, 1334–1345. [CrossRef] [PubMed]

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